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First published online October 5, 2007
Journal of Experimental Biology 210, 3689-3695 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.009126
Cross-modal effects on learning: a seismic stimulus improves color discrimination learning in a jumping spider
1 Environmental Science, Policy and Management, University of California
Berkeley, Berkeley, CA 94720, USA
2 School of Biological Sciences, University of Nebraska, Lincoln, NE 68588,
USA
* Author for correspondence (e-mail: ndv{at}nature.berkeley.edu)
Accepted 9 August 2007
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Summary |
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Key words: avoidance learning, cross-modal interactions, jumping spider, multimodal, receiver psychology, seismic signal
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Hebets and Papaj, 2005;
Partan and Marler, 2005).
While a majority of empirical and theoretical work has thus far focused on
testing content-based hypotheses (e.g.
Johnstone, 1996;
Møller and Pomiankowski,
1993), studies incorporating content-based, efficacy-based and
inter-signal interaction approaches are necessary for a complete understanding
of complex signal function (see Candolin,
2003; Hebets and Papaj,
2005).
Research on inter-signal interactions (i.e. instances where the presence of
one signal influences a receiver's response to a second signal), particularly
cross-modal effects, may be especially important for understanding how a
receiver's sensory, processing and storing capabilities [i.e. `receiver
psychology' (Guilford and Dawkins,
1991)] shape ultimate signal form
(Guilford and Dawkins, 1991;
Rowe, 1999). For example, in
humans, the detectability of sound is improved by an irrelevant light
(Lovelace et al., 2003), and
visual discrimination improves when tactile stimulation is also present
(Spence et al., 1998). Other
studies with humans have demonstrated that a prior sensory stimulus can prime
the nervous system for the perception of future sensory information
(Calvert et al., 1997;
Komura et al., 2005).
Similar cross-modal interactions have been documented in other vertebrate
taxa (e.g. Rowe and Guilford,
1996; Rowe, 2002),
but relatively little remains known about signal interactions in
invertebrates. Nonetheless, some of the few documented cases of cross-modal
interactions in invertebrates come from spiders. For example, the seismic
courtship signal of the wolf spider Schizocosa uetzi has been shown
to influence a female's visual attention
(Hebets, 2005).
Attention-priming effects are also known from the foraging behavior of
salticids, with odor from a prey item priming selective visual attention to
that particular prey type (Clark et al.,
2000; Jackson et al.,
2002).
While such studies have begun to add to our understanding of invertebrate
receiver psychology, no studies to date have explored the potential influence
of complex signaling on invertebrate learning and/or memory. Furthermore, the
cognitive abilities of invertebrates are often underestimated compared with
those of vertebrates. Recent studies have suggested that learning and memory
may play a more important role in arthropod life history than previously
thought (Brembs, 2003;
Edwards and Jackson, 1994;
Elias et al., 2006;
Hebets and Vink, 2007;
Hebets, 2003;
Jackson and Li, 2004;
Skow and Jakob, 2006;
Tibbetts and Dale, 2004).
Thus, here we chose to use an invertebrate predator, the jumping spider
Habronattus dossenus, to determine whether multimodal cues can
influence learning, as has been demonstrated in several vertebrate taxa.
Jumping spiders are diurnally active and most are generalist hunters that
rely heavily on visual and seismic information in both foraging and
intraspecific contexts (Edwards and
Jackson, 1993; Elias et al.,
2005; Forster,
1982a; Forster,
1982b; Hill, 1979;
Jackson and Pollard, 1996;
Land, 1969a;
Taylor et al., 1998). Their
anterior median eyes are adapted for both high spatial resolution
(Eakin and Brandenburger,
1971) and for color vision
(DeVoe, 1975;
Land, 1969a;
Land, 1969b;
Land, 1985;
Peaslee and Wilson, 1989).
These eyes, in combination with three pairs of motion-detecting eyes, result
in the most highly developed visual system in spiders
(Land, 1985). In addition to
their advanced visual capabilities, jumping spiders have also been studied
with respect to their cognitive capabilities. They have been shown to use a
variety of cognitive skills, including complex decision-making, detour routing
and opportunistic smokescreens (using environmental noise to hide stalking
movements) (Edwards and Jackson,
1993; Edwards and Jackson,
1994; Jackson and Li,
2004; Tarsitano and Andrew,
1999; Tarsitano and Jackson,
1994; Wilcox and Jackson,
1998). Of particular relevance to the present study, Nakamura and
Yamashita recently established that jumping spiders are able to learn a
heat-avoidance task based upon colored substrates
(Nakamura and Yamashita,
2000).
Here, using an avoidance learning paradigm, we test the hypothesis that
multimodal cues influence learning in the jumping spider H. dossenus.
Specifically, we test whether the presence of a seismic stimulus influences
color discrimination learning. We trained female H. dossenus to
associate a particular color with heat in the presence and absence of a
seismic stimulus. Habronattus dossenus females were chosen because
they are known to rely on seismic signals in addition to visual signals in the
context of courtship (Elias et al.,
2005; Elias et al.,
2006). We found evidence of a cross-modal effect on learning
– spiders exposed to a seismic stimulus were better able to learn the
association between the color and the heated side compared with those that
received no seismic stimulus.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Experimental arena
We tested the ability of female jumping spiders to associate color with
heat in the presence versus absence of a seismic stimulus. The
experimental arena consisted of two platforms (one seismic-present and one
seismic-absent; see below), each with one side heated
(Fig. 1). The bottom of each
platform was constructed from two 0.125x7.5x15 cm sheets of
aluminum connected with epoxy. Heat was provided by attaching a heating
element underneath one side of each platform (MINCO polyamide heat element,
Minneapolis, MN, USA). For the seismic-present platform, a 1 cm-diameter hole
was drilled at 7.5 cm along the epoxy line between the aluminum plates.
Through this hole, we attached a mini-shaker (Brüel & Kjær Type
4810, Naerum, DK) to the paper that comprised the floor of the platform. Both
platforms were suspended 10 cm above the floor to enable the mini-shaker to
fit below. We placed the mini-shaker in a container with 3 cm of sand to
prevent vibrations from passing to the non-vibration platform
(Fig. 1). One small Petri dish
(diameter=8.8 cm, height=2 cm) was placed in the middle of each of the
seismic-present and seismic-absent platforms, with the open side facing down
to provide an enclosure for the test spiders. In order to introduce the test
spiders into the enclosures, a 1 cm-diameter hole was drilled in the middle of
each Petri dish. The enclosures were visually isolated from one another by a 3
cm-high border of white paper surrounding each Petri dish.
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Visual stimulus
We used two visually distinct colors of construction paper, red and yellow,
for the color discrimination task (BriteHue, Red and Sun Yellow, Cohoes, NY,
USA). The reflectance spectra of these two colored papers are distinct and
have reflectance within the visual sensitivity range of jumping spiders
(Fig. 2)
(Peaslee and Wilson, 1989).
For each color, we cut multiple 8.5 cm-diameter semi-circles. Two
semi-circles, one of each color, were placed together to make a complete
circle that would ultimately provide the floor of the test enclosure. The
bicolor circles were placed on the platforms underneath each Petri dish such
that the junction between the colors rested on top of the epoxy line
(Fig. 1). In the
seismic-present arena, both pieces of paper were taped to the mini-shaker,
which extended through a 1 cm-diameter hole in the center of the arena (see
above). In the seismic-absent arena, the pieces of paper were both taped to
the epoxy at the center of the arena. To control for luminance variation
between arenas, we used one fiber-optic light arm from the same 150 W halogen
light source 10 cm above each arena, and this light source was never
moved.
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Seismic stimulus
For our seismic-present treatment, we used a band-limited broadband seismic
stimulus (1–1500 Hz). This range was chosen based on frequencies known
to be ecologically relevant for H. dossenus
(Elias et al., 2003). The
noise stimulus was created using MatLab (v.6.5.1, Natick, MA, USA). A
mini-shaker was used to produce substrate vibrations in one of the
experimental arenas (Brüel & Kjær Type 4810). The frequency
response of the mini-shaker was flat across all tested frequencies. The
seismic stimulus was broadcast over the entire colored paper substrate, and
the same seismic stimulus was used in every vibration treatment. The intensity
of the stimulus was set based on a series of preliminary trials where we
determined the highest level of seismic stimulus that still maintained normal
spider movement in the arena (based on qualitative observations).
Experimental design
Individual females were randomly assigned to either a seismic-present
(N=11) or seismic-absent (N=11) treatment. Within each of
these treatments, females were assigned either red or yellow as the heated
color. These assignments did not change for an individual female during the
course of the entire experiment. All females were initially run through an
unheated control trial, which allowed us to test for any a priori
color preferences (Gamberale-Stille and
Tullberg, 2001; Rowe and
Guilford, 1996). Next, females were run through 10 training trials
during which heat was present. Finally, they were run through a no-heat test
trial. One seismic-present and one seismic-absent treatment were run
simultaneously during all trials.
Before starting each trial, we measured the temperature of both sides of each arena with a thermocouple. The seismic stimulus was then turned on and two test females were inserted into the center of their respective arenas simultaneously using a syringe with the tip removed. The seismic stimulus was on during the entirety of all trials for the seismic-present group. The center of the arena where the females were initially placed did not have heat (due to the epoxy line), but both colors were present.
As mentioned above, each female was run through an initial control trial in which neither side of the platform was heated (i.e. platform was maintained at room temperature: 23.2±1.3°C, mean ± s.d.). During this 5 min control trial, we scored the number of times an individual ventured into each side of the arena as well as the total number of times the spider jumped. We used the number of times a spider jumped as a measure of the individual's activity level since H. dossenus move around primarily by stepping and jumping (N.D.V. and D.O.E., unpublished observation). Individuals that did not go onto both colors at least once were excluded from the experiment (N=2; one individual from the seismic-present group and one from the seismic-absent group).
For the 10 training trials, one side of each platform was heated to 60°C (59.9±1.1°C), while the other side was maintained at 35°C (35.4±0.8°C). In the first training trial, we dropped spiders onto the heated color to ensure that all spiders were exposed to the heat at the same time. All training trials lasted 5 min. For the training trials, we monitored the number of times an individual ventured onto the heated color, how long it spent on the heated color, and the number of times an individual jumped while on the non-heated color. Individuals often greatly increased the speed and number of jumps while on the heated color, making it difficult to accurately count; we therefore excluded these jumps from the data analysis.
All individuals (N=10 for each treatment group) were run through 10 consecutive training trials, with 15 min separating each trial. During the inter-trial interval we changed the colored papers, cleaned the syringe with 70% ethanol and re-measured the temperature of each side of both arenas. We also rotated the platforms clockwise 90° to control for spiders orienting to visual stimuli above the arena.
Upon completion of 10 training trials, each female was run through a 5-min no-heat test trial. This trial allowed us to determine if the spiders had learned to avoid the color that was heated, rather than just detecting the heat and avoiding the heated side. The test trials took place 20 min after the final training trial, after the platforms were cooled to room temperature (26.2±1.2°C). Females were again introduced into the middle of the arena and we measured whether or not an individual went onto the previously heated color, the delay until an individual went onto the previously heated color, and the total number of individual jumps.
Statistical analysis
We performed four independent-samples t-tests to ensure that the
randomly assigned heated color had no effect on overall activity levels,
number of jumps onto the heated color or duration of time spent on the heated
side. Individual activity levels (number of jumps) in the seismic-present and
seismic-absent treatment groups were analyzed for the control trial, training
trial 1 and trial 10, with independent-samples t-tests. Comparisons
of activity levels for individuals within a treatment group between trial 1
and 10 were analyzed with paired-samples t-tests. The number of times
an individual went onto the heated side, and the duration of time spent on the
heated side in training trial 1 and trial 10 were compared between groups with
independent-samples t-tests and within groups between trials 1 and 10
with paired-samples t-tests. Bonferroni-corrected significance levels
were used in all cases where multiple tests were done on the same data
(P=0.05/number of tests). All tests were performed using SPSS
(v.14.0, Chicago, IL, USA). Results of statistical tests (not including
temperature averages, which are means ± s.d.) are all reported as means
± s.e.m.
Responses in the final test trial were analyzed in two different ways.
First, the number of individuals that went onto the previously heated color
was analyzed with a 
2 test. Since all individuals were
screened for potential color biases in the initial no-heat control trial, we
assume that all 10 individuals in each treatment group would go onto the
previously heated color during the test trial if there was no learning during
the training trials. We therefore set our null hypothesis value to `10' for
the 2 test (N=10 for both treatment groups). A Yates
correction was used in these calculations to control for only one degree of
freedom (Zar, 1998). In a
second analysis, the latency to first contact of the previously heated color
was analyzed using an independent-samples t-test (SPSS v.14.0).
Individuals that never went onto the previously heated color in the test trial
were excluded from this final analysis. In the final test trial, since there
was no heat associated with the previously heated color, individuals had no
incentive to continue to avoid this color. Therefore, we did not analyze the
number of times entered or duration of time spent on the color that had been
previously heated. Instead we considered how long it took an individual to go
onto the previously heated color, if at all, to see if there was any continued
avoidance of the previously heated color, even when no heat cues were
available.
We performed a Shapiro-Wilk W test on all of the variables' distributions to determine whether they fit a normal distribution. To ensure that our t-test results were not affected by any non-normal distributions, we then performed a generalized linear model with quasi-Poisson distribution using R (v.2.5.0, 2007-04-23; CRAN, Vienna, Austria) for all analyses that did not pass the Shapiro-Wilk W test (P=0.05). In all 19 analyses that we repeated, we found the same level of significance with the original t-test and the generalized linear model. We will therefore report our statistics with the t-statistic, which is more commonly known.
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Results |
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Activity levels
There was no difference in activity levels between the seismic-present and
seismic-absent treatment groups across all training trials (present,
N=10, 7.6±4.3 jumps; absent, N=10, 4.8±3.3
jumps; t=–1.635, P=0.119). Individuals in both groups
tended to become less active in later trials, with a greater effect seen in
individuals in the seismic-present treatment (present Trial 1, 4.0±2.2
jumps; Trial 10, 0.4±1.0 jumps; t=4.070, P=0.003;
absent Trial 1, 2.4±3.1 jumps; Trial 10, 0.7±0.823 jumps;
t=1.899, P=0.090). However, when comparing within a trial,
there was no significant difference between individuals in the seismic-present
versus seismic-absent treatments (Trial 1 present, 4.0±2.2
jumps; Trial 1 absent, 2.4±3.1 jumps; t=–1.329,
P=0.200; Trial 10 present, 0.4±1.0 jumps; Trial 10 absent,
0.7±0.823 jumps; t=0.747, P=0.464).
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Number of jumps onto heated color
Seismic-present and -absent treatment groups did not differ in the number
of times individuals went onto the heated color in trial 1
(Fig. 4) (seismic-present,
2.3±1.4 jumps; seismic-absent, 1.5±1.1 jumps; t=1.419,
P=0.173). However, in the tenth trial, individuals in the
seismic-present treatment group went onto the heated color significantly fewer
times than individuals without seismic exposure
(Fig. 4) (seismic-present,
0.3±0.5 jumps; seismic-absent, 1.4±1.3 jumps;
t=–2.569, P=0.019). In addition, within the
seismic-present treatment there was a significant decrease in the number of
times individuals went onto the heated color between Trial 1 and Trial 10
(Fig. 4) (Trial 1,
2.3±1.4 jumps; Trial 10, 0.3±0.5 jumps; t=3.873,
P=0.004). By contrast, in the seismic-absent treatment, there was no
difference between the number of times an individual went on the heated color
in the first and the tenth trials (Fig.
4) (Trial 1, 1.5±1.1 jumps; Trial 10, 1.4±1.3 jumps;
t=0.208, P=0.840).
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Test trial
There was a significant difference between the seismic-present
versus seismic-absent treatment groups in the number of individuals
that went onto the previously heated color during the no-heat test trial
(Fig. 5) (seismic-present,
N=10; seismic-absent, N=10; 2=5.0,
P=0.025). Of the individuals that went onto both colors, there was no
difference in the latency to going onto the previously heated color
(seismic-present, N=6, 62.2±47.3 s; seismic-absent,
N=9, 55.3±56.0 s; t=0.245, P=0.810).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Individuals in the seismic-present treatment initially spent more time on the heated color than did individuals in the seismic-absent treatment. However, over time, seismic-present individuals significantly decreased the amount of time spent on the heated color while no such decrease was observed in the seismic-absent treatment. Despite the initial increased time spent on the heated side by individuals in the seismic-present treatment, we found no differences in overall activity levels (as measured by number of jumps) between the seismic-present and -absent treatment groups. We argue that duration of time spent on the heated color may not be an accurate indication of learning in this type of experimental design as individuals may react differently once introduced to a heated surface, with some `freezing' and others jumping around until they happened to land on the non-heated color. We observed both types of responses in both the seismic-present and seismic-absent treatments.
Although our statistical analyses demonstrate significant differences between the seismic-present and seismic-absent treatments, the variance across trials within a treatment group is notably high. Prior to the start of this experiment, we chose to run 10 training trials and compare the performance of the spiders in the first and last trials. Had we chosen different trial numbers for comparison, our statistical results may have differed but our general conclusions would remain the same (see Figs 3 and 4). Regardless of the specific comparisons, there was a general trend for spiders in the seismic-present group to decrease both how long they spent on the heated color and how often they went onto the heated color. No such trend was evident for the seismic-absent spiders. The most compelling evidence, however, that seismic signals enhanced color-discrimination learning came from the no-heat test trial. In this test trial, seismic-present females showed strong avoidance of the previously heated color while seismic-absent females did not. These findings are the most direct evidence of a cross-modal effect on learning.
The seismic stimulus used in this experiment conveyed no information
regarding which color would be heated (i.e. the differences found across
treatment groups cannot be explained as properties of the seismic stimulus
alone). Instead, these differences resulted from a cross-modal interaction in
which a seismic stimulus influenced some aspect of the receiver's psychology
(e.g. her arousal, perception, attention or retention of visual information).
This study cannot speak to the exact mechanism underlying this cross-modal
interaction, but several possibilities exist. For example, the seismic
stimulus may increase a female's general arousal, making her more inclined to
devote attention to the association between the color and the aversive
stimulus. Alternatively, the seismic stimulus may act to focus a female's
visual attention (see Hebets,
2005), thus enhancing her ability to distinguish between the two
colors and enabling a more accurate association between the color and the
aversive stimulus. The transmission properties of the oak leaf litter
substrate on which H. dossenus is primarily found make it likely that
the spiders are frequently exposed to environmental seismic noise
(Elias et al., 2005).
Consequently, the seismic-present treatment may actually mimic natural
environmental conditions.
One of the more exciting implications of our results relates to our general
understanding of the evolution of aposematic, or warning, coloration. For
example, while the function of conspicuous warning coloration has been
credited to enhance avoidance learning in predators
(Cott, 1940;
Endler and Greenwood, 1988;
Guilford and Dawkins, 1991;
Lynn, 2005), warning displays
of unpalatable prey often combine aposematic coloration with signals in a
secondary modality (e.g. substrate vibrations, airborne vibrations and/or
chemical secretions) (Cokl and
Virant-Doberlet, 2003; Cott,
1940; Poulton,
1890; Rowe and Guilford,
1999a). Recently, it has been proposed that the additional
components of many warning displays may promote the association between the
warning coloration and the non-profitability of the prey item for a predator
(Rowe, 2002;
Skelhorn and Rowe, 2006). This
multimodal facet of warning displays and its interaction with predator
psychology has already received much attention in studies focusing on birds
(Jetz et al., 2001;
Lindstrom et al., 2001;
Rowe, 1999;
Rowe, 2002;
Rowe and Guilford, 1996;
Rowe and Guilford, 1999b;
Skelhorn and Rowe, 2005), yet
these same ideas have not been addressed with invertebrate predators. In
essence, although not previously considered, our results suggest that
invertebrate predators such as jumping spiders could exert strong selection
pressure on the evolution of invertebrate multimodal warning displays, many of
which combine aposematic coloration with broadband vibration or sound
production (Cocroft, 1996;
Cocroft and Rodriguez, 2005;
Hill, 2001;
Masters, 1979). Due to both
their abundance and the amount of prey they are capable of ingesting daily
(for H. dossenus, up to twice their body mass daily; N.D.V.,
unpublished data), generalist invertebrate predators such as jumping spiders
may play a much larger role than vertebrate predators in shaping insect
warning displays – an area of research deserving further
investigation.
In summary, the present study provides some of the first evidence of cross-modal effects on learning in an invertebrate. It offers the first demonstration that seismic stimuli can influence a color discrimination task in a jumping spider and suggests that the complicated cross-modal interactions frequently studied in vertebrate taxa are present in invertebrate groups as well. Although this study does not address the mechanism(s) underlying the observed multimodal effect on receiver psychology, a relatively `simpler' invertebrate system such as jumping spiders may make such future studies more feasible.
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